Oncologic outcomes of colorectal cancer in octogenarians

doi:10.21203/rs.3.rs-3346656/v1

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Oncologic outcomes of colorectal cancer in octogenarians

https://doi.org/10.21203/rs.3.rs-3346656/v1

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Introduction

Octogenarians constitute a growing number of diagnoses for colorectal cancer. However, the optimal treatment for these increasingly vulnerable octogenarians with colorectal cancer remains a challenging issue. The aim of this study was to evaluate the oncologic outcomes of colorectal cancer, comparing octogenarians (>80 years) and younger age (60-79 years).

Methods

A total of 657 patients underwent surgery for colorectal cancer between January 2015 and December 2019 at Gangneung asan hospital. Among them, 491 patients over the age of 60 were enrolled. The exclusion criteria were as follows: only local resection, R1 and R2 resection, absence of data in follow-up, concurrent inflammatory bowel disease, concurrent malignancy, and prior history of malignancy. The patients were divided into two groups according to their age: Octogenarian group (OG, aged > 80 years, n=93), and younger group (YG, aged 60 to 79 years, n=398).

Results

The mean follow-up was 41.8 months (range 1 to 89.4 months). OG showed higher rate of emergency surgery (25.8% vs. 13.6% p=0.004), higher mortality rates (47.3% vs. 25.9%, p<0.001) and received less adjuvant therapy (17.2% vs. 59.5%, p<0.001). Indeed, anastomosis rates in rectal cancer were significantly lower in OG (65.2% vs. 81.1%, p=0.043). Location of tumor, TNM stage, differentiation, retrieved lymph nodes, presence of lymphovascular invasion or perineural invasion, and tumor size were not difference in two groups.

OG had poorer 3-year overall survival (61.2% vs. 81.3%, P<0.001), however, 3-year disease-free survival was comparable between YG (81.2% vs. 87.2%, p=0.177). In multivariate analysis, emergency operation (hazard ratio [HR] = 2.137, 95% confidence interval [CI]: 1.465-3.116, p=0.001), severe complications (HR=1.788, 95% CI: 1.133-2.823, p=0.013), poorly differentiation (HR=2.806, 95% CI: 1.377-5.718, p=0.004), higher TNM stage (HR=6.257, 95% CI: 2.434-16.082, p=0.001), presence of perineural invasion (HR=1.572, 95% CI: 1.092-2.264, p=0.015), and less receiving adjuvant chemotherapy (HR=2.599, 95% CI: 1.735-3.894, p=0.001) were independent factor for worse overall survival. Similarly, Independent associations for recurrence were higher TNM stage (HR=6.887, 95% CI: 2.515-18.864, p=0.001), emergency surgery (HR=2.377, 95% CI: 1.380-4.097, p=0.002), the presence of perineural invasion (HR=1.861, 95% CI: 1.142-3.032, p=0.013), poor differentiation (HR=2.813, 95% CI: 1.221-6.478, p=0.015), and less receiving adjuvant chemotherapy (HR=2.314, 95% CI: 1.315-3.462, p=0.002). Age was not independent factor for recurrence. In OG, patients with no or mild complication (Clavien-Dindo 1-2) had significantly higher 3-year OS (72.8% vs. 38.8%, p<0.001) than patients with severe complications (Clavien-Dindo 3-5).

Conclusion

Try to reduce postoperative complication, screening to avoid emergency setting, and receiving adjuvant treatment would have potential to improve oncologic outcomes of octogenarians with colorectal cancer.

colorectal

octogenarian

oncologic outcome

survival

Colorectal cancer is the fourth most common cancer and the third leading cause of cancer-related deaths in South Korea. The incidence of colorectal cancer increases with age, and approximately 12% of patients are diagnosed at the age of 80 or older [1]. With the recent increase in life expectancy, the incidence of colorectal cancer is expected to continue rising. Octogenarians, or individuals over the age of 80, represent a rapidly growing segment of the population and are at an increased risk of developing colorectal cancer [2]. Despite this increased risk, there is a paucity of data on the oncologic outcomes of colorectal cancer in octogenarians. As a result, the optimal management of this population remains unclear.

Some studies have suggested that elderly patients diagnosed with colorectal cancer have worse outcomes [3–5], while others have shown opposite [6–9]. Moreover, elderly patients are often excluded from clinical trials [10, 11], and there is no consistent standard for the age criteria defining "elderly."

The mainstay treatment for colorectal cancer is radical surgery and combined chemotherapy, but some studies have shown that as patients get older, both radical surgery and chemotherapy are underused [12, 13]. Various factors, such as comorbidities and decreased organ function, make the treatment of colorectal cancer in octogenarians more challenging, and there is a critical need to better understand the oncologic outcomes of this population. Therefore, the aim of this study is to investigate the oncologic outcomes of octogenarians with colorectal cancer and to determine the optimal treatment approach.

Patients

Patients who underwent surgery for colorectal cancer at the Gangneung Asan Hospital between January 2015 and December 2019 were enrolled in this study. A total of 657 patients underwent surgery for colorectal cancer during this period. Among them, 491 patients over the age of 60 were enrolled. The exclusion criteria were as follows: only local resection, R1 and R2 resection, absence of data in follow-up, concurrent inflammatory bowel disease, concurrent malignancy, and prior history of malignancy. The patients were divided into two groups according to their age: Octogenarian group (OG, aged > 80 years, n = 93), and younger group (YG, aged 60 to 79 years, n = 398).

The study protocol was approved by the institutional review board of the Gangneung Asan Hospital (registration no: 2023-01-008), in accordance with the Declaration of Helsinki.

The patients were divided into two groups according to their age: Octogenarian group (OG, aged > 80 years, n = 93), and younger group (YG, aged 60 to 79 years, n = 398). The following patient characteristics were analyzed: age, sex, primary tumor location, ASA classification, pathologic TNM stage, presence of lymphovascular and/or perineural invasion, histologic differentiation, Clavien-Dindo classification, and presence of adjuvant therapy.

For postoperative surveillance, patients were followed routinely at 3- or 6- month intervals for the first 2 years and at 6 month interval thereafter. At each visit, Carcinoembryonic antigen (CEA) levels were assessed, a full history was obtained, and a physical examination was performed. Colonoscopy was performed within 6 months to 1 year following surgery and every 2 or 3 years thereafter. Abdominopelvic computed tomography (APCT) and chest computed tomography (CT) were performed 3 or 6 months after surgery. Unscheduled CT or positron emission tomography scans were performed for patients with increased serum CEA concentrations or patients who were symptomatic.

Statistical analyses

Survival curves were plotted using the Kaplan–Meier method and compared using the log-rank test. The associations between clinical factors and recurrence-free survival were assessed using the Cox proportional hazard regression model. Comparisons between the PG and OG were performed using the chi-squared test or Fisher’s exact test for categorical variables and Student’s t-test for continuous variables. A p-value < 0.05 was considered statistically significant.

The mean follow-up was 41.8 months (range 1 to 89.4 months). Except the patients under the age of 60 (n = 166), the younger group and old age group in our study cohort were 60.1% (397/658) and 14.1% (93/657), respectively.

The profile of the patients who were included in this study is shown in Table 1. OG showed higher rate of emergency surgery (25.8% vs. 13.6% p = 0.004), higher mortality rates (47.3% vs. 25.9%, p < 0.001) and received less adjuvant therapy (17.2% vs. 59.5%, p < 0.001). Indeed, anastomosis rates in rectal cancer were significantly lower in OG (65.2% vs. 81.1%, p = 0.043). Location of tumor, ASA classification, TNM stage, differentiation, retrieved lymph nodes, presence of lymphovascular invasion or perineural invasion, and tumor size were not difference in two groups.

Oncologic outcomes

OG had poorer 3-year overall survival (OS) for all patients (61.2% vs. 81.3%, P < 0.001), however, 3-year disease-free survival (DFS) was comparable between YG (81.2% vs. 87.2%, p = 0.177). Figure 1 presents the 3-year OS, stratified by age groups at each stage. 3-year OS was similar in stages I (100% vs. 97.1%, p = 0.88) and IV (20% VS. 47.9%, P = 0.073), while in stages II (73.3% VS. 83.5%, P = 0.037) and III (51.3% VS. 76.7%, P < 0.001) 3-year OS was significantly lower in the OG. Moreover, there is no significant difference in 3-year DFS between OG and YG, and no difference in each stage (Fig. 2, stage I: 97.3% vs. 100%, p = 0.447; stage II: 91.3% vs. 90.5%, p = 0.788; stage III: 70.8% vs. 78.4%, p = 0.150).

In multivariate analysis, emergency operation (hazard ratio [HR] = 2.137, 95% confidence interval [CI]: 1.465–3.116, p = 0.001), severe postoperative complications (Clavien-Dindo classification > 3, HR = 1.788, 95% CI: 1.133–2.823, p = 0.013), poorly differentiation (HR = 2.806, 95% CI: 1.377–5.718, p = 0.004), higher TNM stage (HR = 6.257, 95% CI: 2.434–16.082, p = 0.001), presence of perineural invasion (HR = 1.572, 95% CI: 1.092–2.264, p = 0.015), and less receiving adjuvant chemotherapy (HR = 2.599, 95% CI: 1.735–3.894, p = 0.001) were independent factor for worse overall survival (Table 2). Similarly, Table 3 demonstrated that independent associations for recurrence were higher TNM stage (HR = 6.887, 95% CI: 2.515–18.864, p = 0.001), emergency surgery (HR = 2.377, 95% CI: 1.380–4.097, p = 0.002), the presence of perineural invasion (HR = 1.861, 95% CI: 1.142–3.032, p = 0.013), poor differentiation (HR = 2.813, 95% CI: 1.221–6.478, p = 0.015), and less receiving adjuvant chemotherapy (HR = 2.314, 95% CI: 1.315–3.462, p = 0.002). Age was not independent factor for recurrence.

Table 1

Clinicopathological characteristics
Variables	60–79 (n = 398)	≥ 80 (n = 93)
Female	135 (34%)	45 (48%)	*0.017
OP type
Open	140 (35.2%)	44 (47.3%)	*0.029
Laparoscopic	258 (64.8%)	49 (52.7%)
OP type			*0.004
Elective	344 (86.4%)	69 (74.2%)
Emergency	54 (13.6%)	24 (25.8%)
Location			0.561
Rt colon	123 (30.9%)	26 (28.0%)
Lt colon	164 (41.2%)	44 (47.3%)
Rectum	111 (27.9%)	23 (24.7%)
ASA classification			*0.031
I-II	201(50.6%)	31 (33.3%)
III	178 (44.8%)	54 (58.1%)
IV-V	18 (4.6%)	8 (8.6%)
Differentiation
Well differentiation	84 (21.1%)	19 (20.4%)	0.984
Moderate differentiation	283 (71.1%)	67 (72.0%)
Others (poor, mucinous)	31 (7.8%)	7 (7.5%)
Stage			0.482
O	3 (0.8%)	0 (0%)
I	88 (22.1%)	14 (15.1%)
II	128 (32.2%)	30 (32.3%)
III	142 (35.7%)	39 (41.9%)
IV	37 (9.3%)	10 (10.8%)
Retrieved LNs	18.5	20.1	0.161
Lymphovascular invasion, yes	144 (36.7%)	35 (37.6%)	0.872
Perineural invasion, yes	92 (23.7%)	24 (25.8%)	0.662
Adjuvant treatment, yes	237 (59.5%)	16 (17.2%)	*<0.001
Tumor size, cm	4.4	5.1	0.246
Clavien-Dindo classification			0.216
1,2	37 (9.3%)	9 (9.7%)
3,4,5	36 (9.0%)	14 (15.1%)
Mortality	103 (25.9%)	44 (47.3%)	*< 0.001
Rectal cancer
Anastomosis, yes	90 (81.1%)	15 (65.2%)	*0.043

Table 2

Univariate and Multivariate analysis of factors asssociated with Overall Survival
Overall Survival
	Univariate		Multivariate
	P - value	HR	95% CI	P - value
Age (group)	0.097
Gender	0.789
Operation type	0.001
elective
emergency		2.137	1.465–3.116	0.001*
Clavien-Dindo classification
0
1,2
3–5	0.04	1.788	1.133–2.823	0.013*
Tumor location	0.510
Rt. colon
Lt. colon
Rectum
ASA classification	0.379
I-II
III
IV-V
Differentiation	0.024
Well
Moderate
Poor/Mucinous		2.806	1.377–5.718	0.004*
Stage	0.001
I
II		6.257	2.434–16.082	0.001*
III		8.693	3.335–22.662	0.001*
IV		24.868	8.964–68.990	0.001*
Lymphovascular invasion, yes	0.101
Perineural invasion, yes	0.042	1.572	1.092–2.264	0.015*
Adjuvant chemotherapy, yes	0.001	0.405	0.287–0.571	0.001*
CI = confidence interval, HR = hazard ratio
* P < 0.05

Table 3. Univariate and Multivariate analysis of factors asssociated with Disease Free Survival

Disease Free Survival
	Univariate		Multivariate
	P - value	HR	95% CI	P - value
Age	0.997
Gender	0.153
Operation type	0.001*
elective
emergency		2.377	1.380–4.097	0.002*
Clavien-Dindo classification	0.827
0–2
3–5
Tumor location	0.326
Rt. colon
Lt. colon
Rectum
ASA classification	0.437
I-II
III
IV-V
Differentiation	0.016
Well
Moderate
Poor/Mucinous		2.813	1.221–6.478	0.015*
Stage	0.001*
I
II		2.726	0.963–7.716	0.059
III		6.887	2.515–18.864	0.001*
Lymphovascular invasion, yes	0.389
Perineural invasion, yes	0.046*	1.861	1.142–3.032	0.013*
Adjuvant chemotherapy, yes	0.055	0.598	0.373–0.959	0.033*
CI = confidence interval, HR = hazard ratio
* P < 0.05

Survival according to postoperative complication

In OG, patients with no or mild complication (Clavien-Dindo 1–2) had significantly higher 3-year OS (72.8% vs. 38.8%, p < 0.001) than patients with severe complications (Clavien-Dindo 3–5, Fig. 2). Cause of death was cancer-related in 12 (27%), due to pneumonia in 6 (13.6%), due to other known causes in 6 (ICH, cardiac arrest, Parkinson, other cancer, sepsis; 13.6%), and unknown in 20 (45.8%) of the deceased patients.

In our study, we observed that octogenarian had worse overall survival (OS) compared to younger patients, but there was no significant difference in disease-free survival (DFS) between the two groups. Additionally, it was noted that the occurrence of severe postoperative complications was associated with decreased overall survival. Furthermore, we found that octogenarian had higher ASA scores and were more likely to undergo surgery in emergency situations when compared to younger patients.

Elderly patients exhibit diverse prognoses based on various morbidities and general conditions. Previous studies have reported lower survival rates among elderly patients after surgery [5, 14], however, other studies demonstrated comparable survival outcomes between octogenarians and younger patients [9, 15, 16]. Octogenarians often present with multiple comorbidities and are susceptible to unpredictable fatal illnesses, making it challenging to establish appropriate comparisons. Moreover, elderly patients frequently experience loss to follow-up, making it difficult to ascertain the precise causes of death. In our study, cancer-related deaths accounted for only about a quarter of all deaths, while deaths due to other causes constituted a quarter, and approximately half of the cases had unknown causes of death. Similarly, in other study [16], surgery-related deaths accounted for approximately 8%, cancer-related deaths for 14%, deaths from other causes for around 20%, and cases with unknown causes of death for about 59%. While lower overall survival among elderly patients can generally be predicted, further research is needed to determine whether these findings specifically pertain to cancer-related outcomes. Furthermore, our study demonstrated that disease-free survival in octogenarians is comparable to that of the younger group. While some studies [5, 15] have reported lower disease-free survival in octogenarians, there are also findings suggesting that disease-free survival is unrelated to age [3, 9]. Because octogenarians may have a variety of causes of death, it is difficult to accurately compare oncologic outcomes. While this may appear to decrease overall survival, it is important to note that disease-free survival is similar to the younger population.

In this study, severe postoperative complications in the octogenarian group were identified as a significant factor associated with decreased survival. Patients who experienced severe complications showed a more than two-fold difference in 3-year overall survival compared to those who experienced only mild complications. These findings are consistent with previous studies [16–18]. Furthermore, there are studies suggesting that octogenarians who survive the first year after surgery demonstrate good long-term survival [3, 9, 19]. Considering that elderly patients often have higher comorbidity burdens and weaker physical resilience, they are more prone to postoperative complications. However, if they can recover well without complications after surgery, elderly patients can achieve oncologic outcomes similar to younger patients. Therefore, it is crucial to prioritize meticulous care to ensure a complication-free recovery in elderly patients, as this can greatly impact their overall prognosis. However, the concept of prehabilitation prior to surgery has not received sufficient attention thus far. As part of this approach, the geriatric assessment evaluates various individual modifiable factors that are relevant to optimizing the patient's condition before undergoing surgery [20]. Furthermore, studies have demonstrated that a multidisciplinary team approach can enhance the postoperative outcomes for frail patients [21].

Octogenarians had a significantly higher rate of undergoing emergency surgery compared to the younger group, and emergency surgical procedures were identified as significant factors associated with decreased overall survival and disease-free survival. These findings align with previous studies [9, 17, 22] that have also reported a higher incidence of emergency surgery in octogenarians and demonstrated unfavorable outcomes associated with receiving emergency surgical interventions. In our country, the colorectal cancer screening programs commence at the age of 50. Consequently, octogenarians have a lower rate of cancer diagnosis through screening compared to younger patients, resulting in a higher proportion of emergency surgeries. This situation is associated with an increased risk of postoperative complications and higher mortality rates.

Consistent with previous studies, our research also observed that octogenarians had a lower rate of receiving treatment and received less aggressive treatment [5, 12, 13, 23–25]. However, several studies [9, 25–27] have provided evidence of the benefits associated with surgical intervention or chemotherapy in octogenarians diagnosed with colorectal cancer. In our study, similar to other research findings, the proportion of octogenarians receiving adjuvant chemotherapy was lower. However, not receiving chemotherapy after surgery was identified as an independent factor associated with worse overall survival. Therefore, considering the patient's general condition, actively pursuing adjuvant chemotherapy is expected to improve overall survival.

This study has several limitations that should be considered. Firstly, the retrospective methodology employed in this study may introduce bias as there could be unknown or unrecorded confounding factors that were not accounted for. Additionally, it is important to note that the results may not be generalizable to the broader older population. The main limitation of this study is its inclusion of only octogenarians who underwent surgical treatment, which may introduce selection bias as healthier patients were more likely to be chosen for surgical intervention. However, despite these limitations, the data from this study suggest that surgical treatment can yield favorable outcomes in octogenarians diagnosed with cancer. In addition, it is important to note that the assessment of patient condition in this study relied solely on the ASA score, which provides limited information about the patients' functional status. Essential aspects such as daily life functioning, frailty, muscle strength, cognitive functioning, general performance, and the presence of sarcopenia were not documented or taken into consideration. These factors could have influenced the outcomes and should be acknowledged as potential limitations of the study.

Authors' Contributions: Soo Young Oh and Jung Yun Park contributed equally to drafting the manuscript and interpreting data; Seong-A Jung, Yong Jae Kwon, Chung Hyeun Ma, Yun Tae Jung, Keong Won Yun, Kwang Hyun Yoon, Jae Young Kwak, Chang Sik Yu contributed to acquisition, analysis of data; KM Yang had the original idea for the paper, gave critical comments, and revised the manuscript. All authors reviewed the manuscript.

Conflict-of-interest statement: The authors have no conflicts of interest, financial or otherwise

No funding was obtained for this study

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Oncologic outcomes of colorectal cancer in octogenarians

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Abstract

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Introduction

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Patients

Statistical analyses

Results

Oncologic outcomes

Survival according to postoperative complication

Discussion

Conclusion

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